Hundreds of nuclear and plastid loci yield insights into orchid relationships

Abstract

Premise of the studyEvolutionary relationships in the species-rich Orchidaceae have historically relied on organellar DNA sequences and limited taxon sampling. Previous studies provided a robust plastid-maternal phylogenetic framework, from which multiple hypotheses on the drivers of orchid diversification have been derived. However, the extent to which the maternal evolutionary history of orchids is congruent with that of the nuclear genome has remained uninvestigated.MethodsWe inferred phylogenetic relationships from 294 low-copy nuclear genes sequenced/obtained using the Angiosperms353 universal probe set from 75 species representing 69 genera, 16 tribes and 24 subtribes. To test for topological incongruence between nuclear and plastid genomes, we constructed a tree from 78 plastid genes, representing 117 genera, 18 tribes and 28 subtribes and compared them using a co-phylogenetic approach. The phylogenetic informativeness and support of the Angiosperms353 loci were compared with those of the 78 plastid genes.Key ResultsPhylogenetic inferences of nuclear datasets produced highly congruent and robustly supported orchid relationships. Comparisons of nuclear gene trees and plastid gene trees using the latest co-phylogenetic tools revealed strongly supported phylogenetic incongruence in both shallow and deep time. Phylogenetic informativeness analyses showed that the Angiosperms353 genes were in general more informative than most plastid genes.ConclusionsOur study provides the first robust nuclear phylogenomic framework for Orchidaceae plus an assessment of intragenomic nuclear discordance, plastid-nuclear tree incongruence, and phylogenetic informativeness across the family. Our results also demonstrate what has long been known but rarely documented: nuclear and plastid phylogenetic trees are not fully congruent and therefore should not be considered interchangeable.

Settling a family feud: a high‐level phylogenomic framework for the Gentianales based on 353 nuclear genes and partial plastomes

“…This latter method is capable of tackling challenges on phylogenetic reconstruction, such as incomplete lineage sorting and longbranch attraction. Since the premise of MSC is unlinked markers, it is mostly used for nuclear markers, although it might be used for organellar data, to evaluate conflict among genes (Pérez-Escobar et al, 2021;Zuntini et al, 2021). Although these two approaches are fundamentally different, they often result in similar topologies for data sets where the underlying signal is strong, as demonstrated by our results (see comparison in Appendix S6) and observed in others groups such as Apiaceae (Clarkson et al, 2021), Myrtales (Maurin et al, 2021), Ochnaceae (Shah et al, 2021), and Sapindaceae (Buerki et al, 2021).…”

A Comprehensive Phylogenomic Platform for Exploring the Angiosperm Tree of Life

“…Much like a “next generation” rbcL , which underpinned so many Sanger sequencing-based plant phylogenetic studies, the Angiosperms353 genes offer opportunities for continuous synthesis of HTS data across angiosperms. The foundational dataset presented here can be re-used or extended for tree of life research at almost any taxonomic scale (Johnson et al 2019; Larridon et al 2019; Van Andel et al 2019; Murphy et al 2020; Pérez-Escobar et al 2020; Shee et al 2020; Slimp et al 2020; Beck et al 2021). Secondly, this is the first phylogenetic project to gather novel HTS data across angiosperms with a stratified taxon sampling at the genus level.…”

“…More than a dozen studies utilising Angiosperms353 probes are already published (e.g. Larridon et al 2019; Howard et al 2020; Murphy et al 2020; Pérez-Escobar et al 2020; Shee et al 2020; Slimp et al 2020; McLay et al in press), and two journal special issues focused on the probe set are in preparation arising from a recent symposium (Lagomarsino and Jabaily 2020). The probe set has also been adopted by the Genomics for Australian Plants consortium (https://www.genomicsforaustralianplants.com/), which aims to sequence all Australian angiosperm genera, coordinating with the PAFTOL project to optimise collective taxonomic coverage.…”

“…Angiosperms353 probes are an open data resource that can be used without the expense of design or access to prior genomic data and have already been successfully applied across different taxonomic scales (e.g. Larridon et al 2019; Murphy et al 2020; Pérez-Escobar et al 2020; Shee et al 2020), including at the population level (Van Andel et al 2019; Slimp et al 2020; Beck et al 2021).…”

A comprehensive phylogenomic study of the monocot order Commelinales, with a new classification of Commelinaceae

“…The number and arrangement of plastid genes, and the substitution rates they exhibit, are all relatively conserved, which made it easier to design primers and recover sequences than for nuclear markers, considering approaches available at the time (e.g., Ness et al, 2011). However, the plastid genome mostly behaves as a single nonrecombining linkage group (Doyle, 1992;Ness et al, 2011), and so all genes within it could be considered to represent the same evolutionary history (Ness et al, 2011;Johnson et al, 2019), which may conflict with the history suggested by nuclear loci (e.g., Johnson et al, 2019;Pérez-Escobar et al, 2021). High-throughput sequencing (HTS) approaches, such as target sequence capture and, in particular, Hyb-Seq (capture + skimming; Weitemier et al, 2014;Dodsworth et al, 2019) result in a wealth of molecular data (both nuclear and organellar) for phylogenetic inference, which could help to clarify relationships across the order, beyond what is possible with plastid markers alone.…”